Chromosome number and sex determination coevolve in turtles

Although much progress has been achieved in understanding the genetic basis of adaptation, the drivers of genome evolution remain obscure. For instance, extensive variation among reptilian genomes continues largely unexplained, yet reptiles hold critical clues about vertebrate evolution. Turtles posses diverse chromosome numbers (2N = 28-66) derived from extensive genomic rearrangements, plus varied sex-determining mechanisms (genotypic and temperature-dependent). Here, we show that rates of evolution in turtle chromosome number are ~20-fold higher along phylogenetic branches where transitions between sex-determining mechanisms also occur, revealing a strong coevolution of these traits and making drift a less likely driver. Directional tests indicate that both traits evolved effectively in synchrony. These events occurred near global extremes in temperature shifts over the last 200 million years, although the role of climate change remains unknown at this point. Two alternative testable explanations for these patterns are proposed. First, selection for sex determination turnover may co-opt mechanisms (e.g., chromatin remodeling) favoring genomic rearrangements. Alternatively, chromosomal rearrangements underlying diploid number evolution may alter gene regulation enabling transitions in sex-determining mechanisms. Our data indicate that the evolution of sex determination is intimately linked to profound genomic changes underlying diploid number evolution, the ecological context of which remains intriguing.